Small molecules demonstrate the role of dynamin as a bi-directional regulator of the exocytosis fusion pore and vesicle release

Mol Psychiatry. 2015 Jul;20(7):810-9. doi: 10.1038/mp.2015.56. Epub 2015 May 5.

Abstract

Hormones and neurotransmitters are stored in specialised vesicles and released from excitable cells through exocytosis. During vesicle fusion with the plasma membrane, a transient fusion pore is created that enables transmitter release. The protein dynamin is known to regulate fusion pore expansion (FPE). The mechanism is unknown, but requires its oligomerisation-stimulated GTPase activity. We used a palette of small molecule dynamin modulators to reveal bi-directional regulation of FPE by dynamin and vesicle release in chromaffin cells. The dynamin inhibitors Dynole 34-2 and Dyngo 4a and the dynamin activator Ryngo 1-23 reduced or increased catecholamine released from single vesicles, respectively. Total internal reflection fluorescence (TIRF) microscopy demonstrated that dynamin stimulation with Ryngo 1-23 reduced the number of neuropeptide Y (NPY) kiss-and-run events, but not full fusion events, and slowed full fusion release kinetics. Amperometric stand-alone foot signals, representing transient kiss-and-run events, were less frequent but were of longer duration, similarly to full amperometric spikes and pre-spike foot signals. These effects are not due to alterations in vesicle size. Ryngo 1-23 action was blocked by inhibitors of actin polymerisation or myosin II. Therefore, we demonstrate using a novel pharmacological approach that dynamin not only controls FPE during exocytosis, but is a bi-directional modulator of the fusion pore that increases or decreases the amount released from a vesicle during exocytosis if it is activated or inhibited, respectively. As such, dynamin has the ability to exquisitely fine-tune transmitter release.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Catecholamines / metabolism
  • Cells, Cultured
  • Chromaffin Cells / drug effects
  • Chromaffin Cells / metabolism
  • Cyanoacrylates / pharmacology
  • Dynamins / antagonists & inhibitors
  • Dynamins / metabolism*
  • Exocytosis / drug effects
  • Exocytosis / physiology*
  • Hydrazones / pharmacology
  • Indoles / pharmacology
  • Kinetics
  • Male
  • Mice, Inbred C57BL
  • Microscopy, Fluorescence
  • Naphthols / pharmacology
  • Neuropeptide Y / metabolism
  • Secretory Vesicles / drug effects
  • Secretory Vesicles / metabolism*
  • Tyrphostins / pharmacology

Substances

  • Catecholamines
  • Cyanoacrylates
  • Hydrazones
  • Indoles
  • Naphthols
  • Neuropeptide Y
  • Ryngo 1-23
  • Tyrphostins
  • dyngo-4a
  • dynole 34-2
  • Dynamins